Understanding Emotions

484 Pages·2006·12.084 MB·English

by  S. Anders, G. Ende, M. Junghofer, J. Kissler and D. Wildgruber (Eds.)

vi
T. Ethofer, Section of Experimental MR of the CNS, Department of Neuroradiology, University of
Tu¨bingen, Olfried-Mu¨ller Str 51, 72076 Tu¨bingen, Germany
V. Ferrari, Department of Psychology, University of Bologna, Viale Berti Pichat, 5-40127 Bologna, Italy
I. Fischler, Department of Psychology, Psychology Building Room 114, University of Florida, P.O. Box
112250, Gainesville, FL 32611, USA
T.Flaisch,DepartmentofPsychology,InstituteofPsychology,UniversityofKonstanz,Universita¨tstrasse
10, 78457 Konstanz, Germany
V.Gazzola,BCNNeuro-Imaging-Centre,UniversityMedicalCenterGroningen,UniversityofGroningen,
A. Deusinglaan 2, 9713 AW Groningen, The Netherlands
D.Grandjean,SwissCenterforAffectiveSciences,UniversityofGeneva,7ruedesBattoirs,1205Geneva,
Switzerland
G. Hajak, Department of Psychiatry, Psychotherapy and Psychosomatics, University of Regensburg,
Universita¨tstrasse 84, D-93053 Regensburg, Germany
A. Hennenlotter,Department ofNeuropsychology,MaxPlanckInstituteforHuman CognitiveandBrain
Sciences, Stephanstrasse 1a, D-04103 Leipzig, Germany
C. Herbert, Department of Psychology, University of Konstanz, P.O. Box D25, D-78457 Konstanz,
Germany
M. Jungho¨fer, Institute for Biosignalanalysis and Biomagnetism, University of Mu¨nster, Mu¨nster 48149,
Germany
A.Keil,DepartmentofPsychology,ZPRBuilding029,C516,UniversityofKonstanz,BoxD23,D-78457
Konstanz, Germany
C.Keysers,BCNNeuro-Imaging-Centre,UniversityMedicalCenterGroningen,UniversityofGroningen,
A. Deusinglaan 2, 9713 AW Groningen, The Netherlands
J. Kissler, Department of Psychology, University of Konstanz, P.O. Box D25, D-78457 Konstanz,
Germany
S.A. Kotz, Department of Neuropsychology, Max Planck Institute for Human Cognitive and Brain
Sciences, Stephanstrasse 1a, 04103 Leipzig, Germany
B. Kreifelts, Department of Psychiatry, University of Tu¨bingen, Osianderstr. 24, 72076 Tu¨bingen,
Germany
K. Kucharska-Pietura, Whichurch Hospital, Cardiff and Value NHS Trust, Cardiff CF4 7XB, UK
P.J. Lang, NIMH Center for the Study of Emotion and Attention, Department of Clinical and Health
Psychology, University of Florida, 2800 SW Archer Road, Building 772, Gainesville, FL 32610, USA
S. Leiberg, Institute of Medical Psychology and Behavioral Neurobiology, University of Tu¨bingen, MEG
Center, Otfried-Mu¨ller-Str 47, 72076 Tu¨bingen, Germany
J. Meinhardt, Ludwig-Maximilian University, Munich, Germany
M. Meyer, Department of Neuropsychology, Institute for Psychology, University of Zurich, Zurich,
Switzerland
J.L. Mu¨ller, Department of Psychiatry, Psychotherapy and Psychosomatics, University of Regensburg,
Universita¨tstrasse 84, D-93053 Regensburg, Germany
S. Paulmann, Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstrasse 1a, 04103
Leipzig, Germany
M.D. Pell, School of Communication Sciences and Disorders, McGill University, Neuropragmatics and
Emotion Lab, 1266 Avenue des Pins Ouest, Montr´eal, QCH3G 1A8, Canada
P. Peyk, Department of Psychology, University of Basel, Basel, Switzerland
H. Pihan, Department of Neurology, Schulthess Klinik, Lengghalde 2, 8008 Zurich, Switzerland
G.Pourtois,NeurologyandImagingofCognition,ClinicofNeurologyandDepartmentofNeuroscience,
University Medical Centre, University of Geneva, Geneva, Switzerland and Swiss Center for Affective
Sciences, University of Geneva, Switzerland
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D.Sabatinelli,NIMHCenterfortheStudyofEmotionandAttention,UniversityofFlorida,Building772
SURGE, 2800 SW Archer Road, Gainesville, FL 32608, USA
K.R.Scherer, Swiss Centerfor AffectiveSciences, University ofGeneva, 7 rue des Battoirs, 1205 Geneva,
Switzerland
U. Schroeder, Klinik Holthausen, Am Hagen 20, D-45527 Hattingen, Germany
H.T. Schupp,DepartmentofPsychology, InstituteofPsychology, UniversityofKonstanz,Universita¨tstr-
asse 10, 78457 Konstanz, Germany
A. Schwaninger, Department Bu¨lthoff, Max Planck Institute for Biological Cybernetics, Spemannstrasse
38, first floor, 72076 Tu¨bingen, Germany
J.Schwerdtner,DepartmentofPsychiatry,PsychotherapyandPsychosomatics,UniversityofRegensburg,
Universita¨tstrasse 84, D-93053 Regensburg, Germany
M. Sommer, Department of Psychiatry, Psychotherapy and Psychosomatics, University of Regensburg,
Universita¨tstrasse 84, D-93053 Regensburg, Germany
M.Spezio,DivisionoftheHumanitiesandSocialSciences,CaliforniaInstituteofTechnology,Humanities
and Social Sciences 228-77, Pasadena, CA 91125, USA
J. Stockburger, Department of Psychology, Institute of Psychology, University of Konstanz, Univer-
sita¨tstrasse 10, 78457 Konstanz, Germany
D.P. Szameitat, Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstrasse 1a, 04103
Leipzig, Germany
H. Tost, Central Institute of Mental Health, J5, Division of Neuroimaging, 68159 Mannheim, Germany
P. Vuilleumier, Neurology and Imaging of Cognition, Clinic of Neurology and Department of Neuro-
science, University Medical Centre, University of Geneva, Geneva, Switzerland and Swiss Center for
Affective Sciences, University of Geneva, Geneva, Switzerland
C. Wallraven, Department Bu¨lthoff, Max Planck Institute for Biological Cybernetics, Spemannstrasse 38,
72076 Tu¨bingen, Germany
S. Wiens, Department of Psychology, Stockholm University, Frescati Hagva¨g, 10691 Stockholm, Sweden
D. Wildgruber, Department of Psychiatry, University of Tu¨bingen, Osianderstr. 24, 72076 Tu¨bingen,
Germany
Preface
Commonsenseandeverydayexperienceimplythatfeelings,affects,andemotionsdominatelargepartsofour
everydaylives andparticularlyour socialinteractions.Emotionsseemtodrivemuchofour behavior,albeit
apparently not always for the good, leading ancient philosophers to reason that we might be better off
without emotions and that, perhaps,the purpose of reason could be the control of these obscure corners of
our innerlives.In the 17th century, Rene´ Descartes proposeda dualismbetween body and mind whichhas
guided much of the Western philosophy and science until recently. Perhaps as a Cartesian heritage, affects,
emotions, and feelings were all viewed as not lending themselves easily to exact scientific study although
Descarteshimselfviewedemotion,unlikereason,ashavingaphysiologicalbase(inhisTraite´despassionsde
l’aˆme,1649,heevenarguedthatthecontrolofthephysicalexpressionofemotionwouldcontroltheemotions
themselves, a view which has repercussions even today, but it is rarely traced back to Descartes).
Recent developments in the rapidly growing discipline of neuroscience, driven by the enormous meth-
odological and technological advances in neurophysiology, neuroimaging, and computational neurosci-
ences,areheraldingashiftofparadigm.Emotionsarenolongerregardedastooelusivetobeapproached
withscientificmethods,andsomehaveproposedthat humansurvivalandsuccess dependcritically onthe
functioning of the neural networks that are thought to underlie affect, emotions, and, perhaps, feelings.
But what are the results of the scientific study of emotion beyond such increasingly commonplace
statements? What are the data that allow us to draw such seemingly simple conclusions? Are these con-
clusions indeed simple? And, most importantly, what are the implications of emotion research on our
understanding of human social interaction and communication?
Researchersfromallbranchesofbehavioralandphysiologicalsciencesaretryingtospecifythemechanisms
that normally guide emotional processing and the malfunctions that may give rise to emotional disorders.
Thepresentvolumebringsmanyofthemtogether,spanningawidespectrumofexperimentalapproaches
in animals and humans; instrumentations from behavioral testing to neurophysiology and neuroimaging;
paradigms from passive, uninstructed stimulus perception to complex social interaction in different
processing domains. The common thrive behind all contributions is to elucidate emotion as a social
phenomenonthatdoesnotaffectindividualsinisolation,butisrapidlyconveyedbetweenindividuals,some
of these processes being implicit and automatic, others being more explicit and conscious.
ThisvolumeistheresultofaconferenceheldinSeptember2004attheFreudentalCastlenearKonstanz
in southwestern Germany. This conference and this volume would not have been possible without the
generoussupportfromtheHeidelbergAcademyofSciencesandHumanitiesinHeidelbergandtheCenter
for Junior Researchers at the University of Konstanz, which is gratefully acknowledged.
May 2006
Silke Anders, Tu¨bingen
Gabriele Ende, Mannheim
Markus Jungho¨fer, Mu¨nster
Johanna Kissler, Konstanz
Dirk Wildgruber, Tu¨bingen
ix
Anders,Ende,Jungho¨fer,Kissler&Wildgruber(Eds.)
ProgressinBrainResearch,Vol.156
ISSN0079-6123
Copyrightr2006ElsevierB.V.Allrightsreserved
CHAPTER 1
Emotion, motivation, and the brain: Reflex
foundations in animal and human research
Peter J. Lang1,(cid:1) and Michael Davis2
1NIMHCenter forthe StudyofEmotion andAttention, DepartmentofClinical andHealth Psychology,University of
Florida, FL 32610-0165,USA
2DepartmentofPsychiatry,BehavioralSciencesandPsychology,EmoryUniversity,YerkesNationalPrimateCenterand
the Centerfor BehavioralNeuroscience, Atlanta, GA30322,USA
Abstract: This review will focus on a motivational circuit in the brain, centered on the amygdala, that
underlies human emotion. This neural circuitry of appetitive/approach and defensive/avoidance was laid
downearlyinourevolutionaryhistoryinprimitivecortex,sub-cortex,andmid-brain,tomediatebehaviors
basic to the survival of individuals and the propagation of genes to coming generations. Thus, events
associated with appetitive rewards, or that threaten danger or pain, engage attention and prompt infor-
mation gathering more so than other input. Motive cues also occasion metabolic arousal, anticipatory
responses, and mobilize the organism to prepare for action. Findings are presented from research with
animals, elucidating these psychophysiological (e.g., cardiovascular, neuro-humoral) and behavioral (e.g.,
startle potentiation, ‘‘freezing’’) patterns in emotion, and defining their mediating brain circuits. Parallel
resultsaredescribedfromexperimentswithhumans,showingsimilaractivationpatternsinbrainandbody
in response to emotion cues, co-varying with participants’ reports of affective valence and increasing
emotional arousal.
Keywords: fear; startle; amygdala; arousal; conditioning; valence
Introduction clear that motivated behavior, prompted by
appetitive or aversive cues, can be similar across
This essay presents a motivational framework, in- themammalianphyla:Whenaratfirstperceivesa
tegrating animal and human data, with the aim of predatory cat, the rodent’s behavioral and phys-
explicating the biological foundation of human iological reactions are very much like those of a
emotion. The raw data of emotion are threefold: human who, for example, is abruptly aware of an
affectivelanguage,behavior,andphysiology(Lang, intruder in her/his home. Both species initially
1985,1994).Theemphasishereis on the lattertwo ‘‘freeze,’’ and both show parallel changes in heart
data sources — considering emotion’s actions and rateandrespiration.Bothreleasesimilarchemicals
physiologytobefoundedonevolvedneuralcircuits into their blood stream. In each case these events
that are shared by humans and other animals. prompt attention to the potential threat and a
We cannot know if animals experience emotion readying of the body for defensive action. Fur-
in the same way that humans do. However, it is thermore, if an animal or a human escapes the
danger, brain circuits change: The survivor will
(cid:1) have learned to react to tell-tale-signs of the po-
Corresponding author. Tel.: [phone]; Fax: +1-352
392-6047;E-mail:[email protected]fl.edu tential predator, and to be aroused and be more
DOI:10.1016/S0079-6123(06)56001-7 3
4
wary. These adaptive patterns of behavior have Affective valence and arousal
been carefully preserved in evolution because they
are successful in promoting survival. Significantly, The motivated behavior of a simpleorganism such
it is in anticipation of, or subsequent to, these astheflatwormcanbealmostentirelycharacterized
survival situations that humans report the most by two survival movements: Direct approach to
intense emotional experiences. Such reports occur appetitive stimuli and withdrawal from aversive
when motivational systems (reflexive, goal-rele- stimuli (Schneirla, 1959). These are the only avail-
vant behaviors and their determining neural cir- able tools in achieving consummation or escape.
cuits)areactivated,butactionisdelayed,orinthe Thismodestrepertoireiswoefullyinsufficient,how-
aftermathofsuchactions,orwhensignsorsignals ever,formorecomplexspeciesthatmustimplement
appear that recall previous encounters. Thus, many critical sub-goals and cope with a richly per-
much can be learned about the biological founda- ceived sensory environment. Humans have proved
tion of expressed emotion by studying how hu- to be successful survivors, seeming to surmount
mansandlesscomplexanimalsconfrontappetitive niche limitations, adapting readily to a greater
or aversive events. variety of environments. Much of this human suc-
cess can be attributed to language — the ability to
Working on a definition of emotion communicate, to manipulate symbols in problem
solving, and to label and catalog our experience of
Emotioncannotbeoperationallydefinedbyasingle the world. Although language is not the major fo-
measure. Emotions involve multiple responses that cus of this discourse, it is a primary way through
are variously sequenced in time. Events that are which we infer emotional experience in others.
pleasant/appetitive or aversive/threatening initially Thus, the relationship between emotion’s language
engageheightenedattention.Theypromptinforma- and motivationally determined behavior and phys-
tion gathering, and do so more readily than other iology merits a careful prefatory consideration.
less motivationally relevant cues. Motive cues also The language of emotion includes thousands of
occasion general metabolic arousal, anticipatory words with myriad shades of feeling, degrees of
responses that are oriented towards the engaging redundancy, and shared meaning. Faced with this
event, and neuromuscular mobilization of the body plethora,philosophers,psychologists,andpsycho-
for action. These reflex reactions are differently linguists have all tried to condense the list into a
paced and form different patterns, reflecting a few primary emotions, or alternatively, to define
changingorganismicstateaspunishmentorreward dimensions of meaning that might underlay this
become more imminent, and specific goal-oriented vast vocabulary.
actions are deployed. Reports of emotional experi- The view that affects — subjective reports of ex-
enceoccurinthecontextoftheseresponseevents,or perienced emotion — might be organized under a
with their inhibition or delay, but correlations with limitednumberofoverarchingfactorswasproposed
anyspecificaffectivereportarenotoriouslymodest. byWundt(1896)inthe19thcentury.Contemporary
In this chapter we will try to explicate what is studiesofnaturallanguagecategories(Shaveretal.,
special about emotional information processing in 1987; Ortony et al., 1988) suggest that emotional
the brain. We will propose that neural networks knowledge is hierarchically organized, and that the
underlying expressed emotion include direct con- superordinatedivisionisbetweenpositivity(pleasant
nections to the brain’s primary motivational sys- states: love, joy) and negativity (unpleasant states:
tems,appetitiveanddefensive.Theseneuralcircuits anger,sadness,fear).Osgoodandhisassociates(e.g.,
were laid down early in evolutionary history: In Osgood etal.,1957),usingthesemanticdifferential,
primitive cortex, sub-cortex, and mid-brain. They showed that emotional descriptors were distributed
determine the deployment of attentional resources, primarily along a bipolar dimension of affective
systemic mobilization, approach, and defensive valence — ranging from attraction and pleasure to
behaviors, and the formation of conditioned asso- aversion and displeasure. A dimension of activation
ciationsfundamentaltothe survivalofindividuals. — from calm to aroused — also accounted for
5
substantialvariance.Otherinvestigatorshavedrawn habituates (Sokolov, 1963). Cues to appetite or
similar conclusions from factor analysis of verbal aversion, however, lead to systemic adjustments
reports(e.g.,MehrabianandRussell,1974;Tellegen, that facilitate sustained perceptual processing. For
1985), and even, of facial expressions (Schlosberg, example,ananimal(reptileormammal)orientingto
1952). No other factors have ever approached the appearance of a distant predator shows a pro-
the generality and significance of these two simple found deceleration in heart rate — ‘‘fear brad-
variables. ycardia’’ — not found in response to other events
Weshouldnotbetoosurprised,perhaps,tolearn (Campbell et al., 1997). ‘‘Freezing’’ — a statue-like
that affective valence and arousal find a parallel in inhibition ofmovement —accompanies thechange
motivational theories based on conditioning re- in heart rate, along with increased overall sensory
searchwithanimalsand humans.Konorski(1967), acuity. If the predator approaches (shows stalking
for example, founded a motivational typology of behavior), somatic and autonomic activation in-
unconditionedreflexes,keyedtothereflex’ssurvival creases progressively, culminating in defensive ac-
role. Exteroceptive reflexes were either preservative tion. Humans show similar attention and action
(e.g., ingestion, copulation, nurture of progeny) or readiness when confronted with motivational cues
protective (e.g., withdrawal from or rejection of (inlifeandinthelaboratory)respondingreflexively
noxiousagents).Hefurthersuggestedthataffective evenifstimuliarenotactualevents,butmediarep-
states were consistent with this bi-phasic typology: resentations. In fact, stories, pictures, and films all
Preservativeemotionsincludesuchaffectsassexual prompt patterns of bodily change in observers that
passion, joy, and nurturance; fear and anger are co-varywiththeratedaffectivevalence(pleasantor
protective affects. Dickinson and Dearing (1979) unpleasant) and arousal (intensity) of their emo-
developed Konorski’s dichotomy into a theory of tional experience.
two opponent motivational systems, aversive and
attractive,eachactivatedbyadifferent,butequally
wide range of unconditioned stimuli, determining Emotional perception
perceptual-motor patterns and the course of learn-
ing. In this general view, affective valence is deter- Inrecentyears,the psychophysiologyof emotional
mined by the dominant motive system: The perception has been systematically studied, using a
appetitive system (preservative/attractive) prompts set of standard photographic picture stimuli, cali-
positiveaffect;thedefensesystem(protective/avers- brated for affective response. There are currently
ive)isthesourceofnegativeaffect.Affectivearousal nearly 1000 pictures in the International Affective
reflects the ‘‘intensity’’ of motivational mobiliza- PictureSystem(IAPS—Langetal.,1999)ratedfor
tion, appetitive or defensive, determined mainly by experienced pleasure and arousal by a large nor-
degreeofsurvivalneedandtheimminenceorprob- mativesubjectsample.Arepresentativedistribution
ability of nociception or appetitive consummation. of IAPS pictures is presented in Fig. 1 (Bradley,
Fromthisperspective,individualreportedemotions 2000) located ina Cartesian space formed by inde-
would be based on differing, situation-determined pendent dimensions of rated pleasure and arousal.
actiondispositions, as‘‘fear’’indicatesa disposition Similar distributions have also been obtained for
to avoid or escape and ‘‘anger’’ is a disposition to collections of acoustic stimuli (International Affec-
attack. tiveDigitizedSounds(IADS):Bradleyetal.,1998a)
as well as verbal materials (Affective Norms for
English Words (ANEW): Bradley et al., 1998b).
Attention, perception, and emotion Studies of IAPS picture stimuli have uncovered
highlyreliablepatternsofphysiologicalandbehavi-
For both humans and other animals, the first reac- oralresponsesthatvaryconsistentlywiththefactor
tiontoanycueisreflexive,directionalorientationto structure uncovered in studies of emotional lan-
the stimulus (Pavlov, 1927). If the input is motiva- guage (see Fig. 1: Greenwald et al., 1989, 1998;
tionally irrelevant, this ‘‘orienting reflex’’ rapidly Bradley et al., 2003). Thus, when affective valence
6
Fig.1. Intheupperrightofthefigure,picturesfromtheInternationalAffectivePictureSystem(Langetal.,1999)areplottedinatwo-
dimensional(Cartesian)space.Picturelocationisdefinedbymeanratingsofjudgedpleasureandemotionalarousalasreportedbya
normativesample.Thevectorsintheupperandlowerportionsoftheaffectivespacedescribehypothesizedincreasingactivationlevels
inappetitiveanddefensivemotivationthatco-varywithreportedarousal.Theotherthreequadrantsofthefigurecontaingraphic
representationsoftheco-variationbetweenphysiologicalreactionstoasampleofthesepicturestimuliandself-ratingsoftheemotional
experienceofresearchparticipants.Picturesarerankorderedontheabscissabyeithereachparticipant’sratingsofaffectivevalenceor
theirratingsofaffectivearousal.Themeanchangeincorrugatormuscleactivity(topright)andheartrate(bottomright)arepresented
acrossrankedratingsofaffectivevalence(pleasure).Meanskinconductanceresponsesandcorticalevent-relatedpotentials(bottom
right)areplottedasafunctionofrankedaffectivearousalrating.Thecorrelationsareinallsignificantcases(po0.01).
ratings are ranked by picture from the most to the linearly as pictures are rated as more unpleasant;
least pleasant image, for each subject, facial muscle conversely, zygomatic (smile) muscle activity
activity during picture viewing shows a strong increases with judged pleasantness. Heart rate is
monotonic relationship with levels of affective va- also responsive to differences in affective valence:
lence: Corrugator (frown) muscle action increases Unpleasant pictures generally prompt marked
7
deceleration during viewing (recalling the ‘‘fear participantscontrolviewingtime,theylooklonger
bradycardia’’ seen in animals), more pronounced at emotionally arousing pictures, both pleasant
thanthatseenwhensubjectsviewpleasantpictures. and unpleasant, than at neutral pictures (Lang
Otherphysiologicalresponsesvarywithchanges et al., 1993). This latter relationship is not found,
in rated emotional arousal, rather than affective however, if pictures evoke very high levels of dis-
valence.Skinconductance—agoodgeneralindex tress: When phobics view pictures specific to their
of autonomic activation — increments monoton- fear, viewing time is dramatically reduced (see
icallywithincreasesinrated arousal,regardlessof Hamm, et al., 1997). They also show heart rate
picturevalence.Electroencephalographicmeasure- acceleration (rather than deceleration), consistent
ment(EEG)showsadistinct,voltage-positivecor- with a precipitous increase in defense motivation
tical response evoked directly by the picture and mobilization for active escape.
stimuli. This is also positively correlated with Asthephobiadataimply,relationshipsbetween
stimulus arousal (i.e., it is similarly enhanced for specific measures can vary widely for individuals
both pleasant and unpleasant arousing pictures: and to some extent between particular groups.
Cuthbert et al., 2000; Keil et al., 2002). These Gender differences, for example, are highly relia-
measures appear to index the intensity or activa- ble: Pleasantness ratings covary more closely with
tionlevelofthecurrentmotivationalstate,butare facial muscle activity in females than in males; on
silent about motivational direction (i.e., appetitive the other hand, skin conductance changes are
or defensive). more closely correlated with arousal ratings in
Behaviors elicited in the context of emotional males than in females (Lang et al., 1993).
picture perception (in reaction to secondary stim- Theresultsoffactoranalysesofaffectself-report,
uli) also covary with motivational engagement. physiological, and behavioral measures are pre-
Whenfirstexposedtoanewpicture,reactiontime sented in Table 1. The data were obtained from
responses to probes are significantly slower for large groups of young, healthy participants. The
emotionallyarousingthanforaffectivelycalmpic- obtained two-factor solution is clearly very strong:
tures(Bradleyetal.,1992).Thesedatasuggestthat Pleasantness ratings, heart rate, and facial muscles
new activating images may require more attentio- load on a first, affective valence factor; arousal and
nal resources at encoding. Furthermore, when interestratings,viewingtime,skinconductance,and
Table1. Factoranalysesofmeasuresofemotionalpictureprocessing
Measure Factor1(Valence) Factor2(Arousal)
Sortedloadingsofdependentmeasuresonprincipalcomponents(Langetal.,1993)
Valenceratings 0.86 –0.00
Corrugatormusclea –0.85 0.19
Heartrate 0.79 –0.14
Zygomaticmusclea 0.58 0.29
Arousalratings 0.15 0.83
Interestratings 0.45 0.77
Viewingtime –0.27 0.76
Skinconductance –0.37 0.74
Sortedloadingsofdependentsmeasuresonprincipalcomponents(Schuppetal.,1994)
Valenceratings 0.89 0.07
Corrugatormusclea –0.83 –0.10
Heartrate 0.73 –0.02
Arousalratings –0.11 0.89
Corticalslowwave –0.06 –0.79
Skinconductance 0.19 0.77
aBioelectricpotentialsfrommusclesthatmediatefacialexpression.
8
cortical EEG load on a second, affective arousal Neural substrates of emotion: Attention, action and
factor. The cross-loadings for all measures are very the role of the amygdala
low. The data are consistent with the view that re-
ported affective experience is determined in signifi- Much recent research has shown that a brain area
cantpartbytheindividual’smotivationalstate.That calledtheamygdalaisacrucialstructureinaneural
is,negativeaffectivevalence(unpleasantexperience) network that mediates motivated attention and
is associated with activation of the defense system; preparationforaction.Inman,thisalmond-shaped
positivevalence(pleasantfeelings)isassociatedwith structureliesdeepinthebrain’stemporallobe.Itis
activation of the appetitive system. Reports of composed of several different nuclei that serve
arousal are associated with both states, reflecting different network functions. The basolateral am-
an increase in incentive strength and organismic ygdala (Bla), which includes the lateral, basal and
mobilization. The motivational states elicited by basomedial nuclei, isof particular significance, asit
these affective cues (and the somatic, cortical, and receives information from the thalamus, hippocam-
autonomic substrates of their perception) appear to pus,andcerebralcortex(seeMcDonald,1998),and
be fundamentally similar to those occurring when then projects (Fig. 2) to other amygdala nuclei, as
othercomplexanimals‘‘stop,look,andlisten,’’sift- well as to targets elsewhere in the brain relevant to
ing through the environmental buzz for cues of emotional memory and action. The Bla’s projec-
danger, social meaning, or incentives to appetite. tions to the central nucleus of the amygdala (CeA)
Fig.2. Schematicdiagramoftheoutputsofthebasolateralnucleusoftheamygdalatovarioustargetstructures,andthesubsequent
outputs and targets of the amygdala’s central nucleus (CeA) and the lateral basal nucleus of the stria terminalis (BNST: The
‘‘extended’’amygdala).Knownandpossiblefunctionsoftheseconnectionsarebrieflydescribed.
9
and the bed nucleus of the stria terminalis (BNST; vigilance and superior signal detection found in
or ‘‘extended amygdala’’) are relayed from these the attentional phase of emotional processing.
sites to specific hypothalamic and brainstem target Asalreadynoted,sensoryorientationtothreatin
areas that mediate most of the visceral and striate mammals and reptiles is accompanied by a pro-
muscle events that index emotional processing. found decrease in heart rate (‘‘fear bradycardia’’:
Their projections target lateral hypothalamus — a Campbell et al., 1997). Heart rate decrease is asso-
key center activating the sympathetic branch of the ciatedwithattentioninhumans(GrahamandClif-
autonomic nervous system in emotion (LeDoux ton, 1966) and furthermore, a greater deceleration
etal.,1988).Inaddition,directprojectionsfromthe is generally found in response to stimuli judged to
BNSTgotothedorsalmotornucleusofthevagus, be unpleasant (Bradley, 2000; Lang et al., 1993).
the nucleus of the solitary tract, and the ventrolat- Several lines of research suggest that this cardiac
eral medulla. These brainstem nuclei are known to response can be mediatedby the centralnucleus of
regulate heart rate and blood pressure (Schwaber the amygdala. During Pavlovian aversive condi-
etal.,1982),andmaythusmodulatecardiovascular tioning in rabbits, one sees a rapid development of
responses in emotion. Projections to the par- conditioned bradycardia. Pascoe and Kapp (1985)
abrachial nucleus are likely to be involved in emo- found a high correlation (.71) between the firing
tion’s respiratory changes (with additional, perhaps frequency of individual neurons in the amygdala’s
indirect effects on the cardiovascular system), as centralnucleusandextentofheartratedeceleration
electricalstimulationandlesionsofthisnucleusalter toaconditionedstimulus.Furthermore,thecentral
breathing patterns. Finally, indirect projections nucleus of the amygdala could have indirect, but
from the amygdala’s central nucleus to the para- widespread, effects on corticalactivity — mediated
ventricular nucleus (via the BNST and preoptic by projections to cholinergic neurons that in turn
area) may mediate neuroendocrine responses that project to the cortex (Kapp et al., 1992). This path
are particularly prominent when emotional stimuli may account for changes in the EEG waveform,
are sustained. perhaps associated with enhanced sensory process-
ing, acquired during Pavlovian aversive condition-
ing at the same rate as conditioned bradycardia.
Attention, vigilance, and conditioned fear
Motor behavior
During emotional stimulation,projections from the
central nucleus or BNST to the ventral tegmental
Emotion’s attentional phase is characterized by im-
areaappeartomediateincreasesindopaminemeta-
mobility,‘‘freezing,’’mediatedintheratbyamygdala
bolites in the prefrontal cortex (Goldstein et al., (CeA) projections to the ventral periacqueductal
1996). Cells in the locus coeruleus, which release
gray. In the action phase, projections to the dorsal
norepinephrine into the brain, are also activated, periacqueductal gray appear to mediate fight/flight
perhaps mediated by projections to its dendritic responses (Fanselow, 1991). As norepinephrine and
field, or indirectly, via projections to the par- serotonin facilitate excitation of motor neurons
agigantocellularis nucleus (Redmond, 1977; Aston-
(McCallandAghajanian,1979;WhiteandNeuman,
Jones et al., 1996). Furthermore, there are direct
1980), rapid defensive action could be mediated by
projections to the lateral dorsal tegmental nucleus lateralBNST activationofnorepinephrinereleasein
and parabrachial nuclei. These latter nuclei have
thelocuscoeruleusorviaitsprojectionstoserotonin
cholinergicneuronsthatprojecttothethalamusand
containing raphe neurons.
couldmediateincreasedsynaptictransmissionofits
sensory relay neurons. The sensory thalamus is, of
course,aprimaryprocessorofenvironmentalinput. Amygdala stimulation
Thus, this sequence of projections, by augmenting
cholinergic activation and facilitating thalamic Electrical stimulation of the amygdala, or a
transmission, may contribute to the increased bnormal electrical activation via temporal-lobe